Download Linking Biodiversity Above and Below the Marine Sediment

Articles
Linking Biodiversity Above
and Below the Marine
Sediment–Water Interface
PAUL V. R. SNELGROVE, MELANIE C. AUSTEN, GUY BOUCHER, CARLO HEIP, PATRICIA A. HUTCHINGS,
GARY M. KING, ISAO KOIKE, P. JOHN D. LAMBSHEAD, AND CRAIG R. SMITH
C
hanges in the marine environment are evident on
a global scale (McGowan et al. 1998), and although biodiversity in the oceans is poorly described, abundances and
distributions of both commercially exploited (Safina 1998) and
nonexploited (Pearson and Rosenberg 1978) species have
changed. Not only have major changes occurred but the rate
of alteration of marine ecosystems appears to be accelerating
(e.g., Cohen and Carlton 1998). Unfortunately, the impact of
these changes in biodiversity on the basic functioning of marine ecosystems remains uncertain, as does the oceans’ capacity
to withstand multiple human disturbances (Snelgrove et al.
1997). The dynamics of many marine ecosystems, as well as
of important fisheries, depend on close coupling between
benthic (bottom living) and pelagic (water column) organisms (Steele 1974). Our knowledge of the natural history of
these systems remains limited, and scientific interest in mapping the diversity of organisms and how they live has been
marginalized in recent years. Given the expanding sphere of
human influence on the oceans, it is imperative to understand
not only patterns of biodiversity and the extent to which
changes in biodiversity are occurring but also how changes in
the benthic and pelagic realms might affect each other. The
oceans provide many important ecosystem services, including production of food, stabilization of shorelines, trapping
and removal of excess nutrients and pollutants, and cycling
of nutrients and organic matter. How does biodiversity
above and below the sediment–water interface influence
these services, and will biodiversity loss on one side of the interface impact the services provided by the other?
THE ORGANISMS LIVING ON THE OCEAN
FLOOR ARE LINKED TO THOSE LIVING IN
THE OCEAN ABOVE, BUT WHETHER OR
HOW THE BIODIVERSITY IN THESE TWO
REALMS IS LINKED REMAINS LARGELY
UNKNOWN
The sediment–water interface (SWI) in marine ecosystems
is one of the most clearly defined ecological boundaries on
Earth. Many organisms in the water column, such as salps
and jellyfish, have flimsy and attenuated morphologies that
allow near-neutral buoyancy in their fluid habitat, where horizontal advection, turbulent mixing, and gravitational settling dramatically influence the relative distributions of
organisms and transport of materials around them. Physical and chemical gradients in the water column (e.g., from
oxic to anoxic waters) occur over scales of meters or more.
Surface waters are always well oxygenated, and waters
near the bottom are usually well oxygenated except where
large amounts of decomposition occur and bacterial respiration drives down oxygen concentration. Below the
sediment–water interface, the morphology of organisms and
the physical attributes of the environment differ markedly.
Paul V. R. Snelgrove (e-mail: [email protected]) is an associate chair in fisheries conservation in the Fisheries and Marine Institute,
Memorial University of Newfoundland, St. John’s, Newfoundland, Canada A1C 5R3. Melanie C. Austen is a senior research scientist in the marine
biodiversity group at the Centre for Coastal and Marine Sciences Plymouth Marine Laboratory, Plymouth PL1 3DH, United Kingdom. Guy Boucher
is a research director of the National Center for Scientific Research in the Biology of Marine Invertebrates Laboratory, National Museum of Natural History, 75231 Paris, France. Carlo Heip is acting director of the Netherlands Institute of Ecology and director of research of the Centre of Estuarine and Coastal Research of the Netherlands Institute of Ecology, 4400 AC Yerseke, Netherlands. Patricia A. Hutchings is a principal research
scientist at the Australian Museum, Sydney NSW, Australia 2010. Gary M. King is a professor of microbiology and marine science at the Darling
Marine Center, University of Maine, Walpole, ME 04573. Isao Koike is a professor at the Ocean Research Institute, University of Tokyo, Tokyo 164,
Japan. P. John D. Lambshead is a principal research scientist in the Nematode and Polychaete Research Group, Natural History Museum, London
SW7 5BD, United Kingdom. Craig R. Smith is a professor in the Department of Oceanography, University of Hawaii at Manoa, Honolulu, HI 96822.
© 2000 American Institute of Biological Sciences.
1076 BioScience • December 2000 / Vol. 50 No. 12
Articles
Even the muddiest sediments are more
like solids than seawater, with mixing
frequently controlled by biological activities such as feeding and burrowing
(bioturbation). Infauna, the organisms living within sediments such as
polychaete worms or shrimp-like crustaceans, are usually denser than those
in the water column because surrounding sediments remove the problem of avoiding sinking. Body forms
are more robust to permit the burrowing that can be essential to existence. Physical and chemical gradients
are steep; for example, the transition
from oxic-to-anoxic sediments often
occurs on millimeter scales. In addition, organisms and nutrients are
usually orders of magnitude more
abundant in sediments than in overlying waters; materials sinking from
above accumulate on sediments and
fuel bottom-living organisms.
Because of differing ecosystem
structure above and below the SWI,
the ecologists who study these domains must use different techniques,
and often ask different research questions. This specialization can often
lead to scientific isolation of the two
domains. For example, a recent workshop of hydrozoan specialists emphasized the problem of duplication
of species descriptions by those focusing on benthic versus pelagic stages
of a given species (Boero and Mills
1999). Despite the dichotomy in research communities, there are numerous strong connections across the
SWI. These are seen not only in life cycles (e.g., Marcus and Boero 1998)
Figure 1. Schematic representation of above–below sediment linkages in shallow
but also in the dissolved and particuhabitat with structural vegetation (top), coastal areas without structural vegetation
late materials that routinely cross the
(middle), and open ocean systems (bottom). Stippled area denotes photic zone where
water–sediment boundary (Figure 1).
photosynthesis is occurring.
Chemical energy for marine benthic systems is often provided by
single-celled and chain-forming phytoplankton (algae),
and salt marsh plant detritus, may be carried away from the
which are the dominant primary producers in the ocean. Livnearshore environment before sinking to the bottom and
ing cells may sink or be physically mixed to the bottom, or
providing another potential food source. A less predictable
dead cells may sink to the bottom as phytodetritus. In surbut sporadically important food source for the benthos is carface waters, crustaceans and other groups of zooplankton
casses of fish, whales, and invertebrates that sink from the
feed on phytoplankton and defecate fecal pellets, which
water column above (Smith et al. 1998). The benthos, in turn,
may then sink to the bottom and provide undigested phyhelps to recycle the nutrients required by the planktonic altodetritus and associated bacteria as an important food
gae that fuel much of the ocean’s benthic and pelagic prosource for the benthos. Plant material from coastal enviduction (Graf 1992). Clearly, individuals of different species
ronments, such as seagrass, mangal (mangrove habitat),
traverse and/or impact other species on more than one side
December 2000 / Vol. 50 No. 12 • BioScience 1077
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of this interface, but is biodiversity above and below the SWI
interface linked? The goals of this article are to summarize
the state of knowledge concerning connections and directionality of effects between organisms living above and below the SWI that may be related to biodiversity, to identify
or hypothesize connections that are likely to be important,
and to outline approaches that might clarify mechanisms of
across-interface biodiversity linkages. Specifically, are there
“water column-down” effects in which pelagic diversity affects sedimentary diversity? Are there “sediment-up” effects
in which the reverse is true? The potential impact of global
change processes on these relationships is reviewed separately
(Smith et al. 2000).
For this article, we separate marine ecosystems into three
distinct groups based on potential relationships between
above- and below-SWI biota. First, shallow sedimentary
systems with structural vegetation such as mangals, salt
marshes, and seagrass beds support unique faunas and
processes; within this grouping, we will also briefly consider
green algal and kelp beds, which are primarily hard substrate
communities but occasionally contain sediments. Second,
we consider nonvegetated shallow-water coastal systems in
which wind and turbulence mix the water column to the SWI
during part of the annual cycle. These habitats encompass
highly dynamic environments, such as sand beds on exposed coastline, and relatively quiescent muddy areas in
sheltered regions that are physically disturbed only rarely. Finally, we consider open ocean systems in which mixing and
light never penetrate to the SWI. We also divide organisms
into those that occur above or below the SWI, and treat organisms that live predominantly on or above the sediment
surface (seagrasses and green algae, salt marsh plants, pelagic
organisms, hyperbenthos, etc.) as above-SWI. In making this
distinction, we acknowledge that many benthic species have
a pelagic reproductive dispersal stage, and some above-SWI
species have a below-SWI component (e.g., salt marsh grass
roots) or life stage (e.g., hydrozoans). In addition, we confine our discussion of linkages to sedimentary benthic systems and largely ignore hard substrate communities, coral
reefs, and kelps except where sediments are present. We
also acknowledge that the information presented declines
as a function of ocean depth; this pattern reflects not only
the differences in present knowledge but also our best guess
as to the strengths of linkages between above- and belowsediment biodiversity.
The meaning of biodiversity
In keeping with common usage and the Convention on Biological Diversity, we define biodiversity in the broadest
sense to encompass the variability of nature in terms of genetics, species, habitats, and even ecosystems. This usage is
kept deliberately broad and is not confined to a unit as
such. Some of the best examples of above–below linkages that
we will summarize are known to directly involve only one
or a few species; nevertheless, we feel that they do represent
an aspect of biodiversity. In more specific terms, species
1078 BioScience • December 2000 / Vol. 50 No. 12
richness refers to numbers of species in an area, and composite
diversity refers to measures of species diversity that incorporate not only species number but also how individuals are
apportioned among those species (evenness). Common
measures of composite diversity include the Shannon–
Weiner (H) diversity index and Hurlbert rarefaction (expected species, or E[Sn]). Where possible, we will use the specific measure of diversity given in a particular study, but the
use of different measures in different studies can make comparisons difficult. Moreover, a change (or lack of change) in
one measure does not always mean there is no change in another aspect of diversity. We also consider diversity on multiple scales, following the conceptualization of Whittaker
(1972). Within this framework, alpha diversity is the diversity within a small, relatively homogeneous area, which for
the benthos is operationally the smallest scale sampled (the
spatial scales of the smallest core sampler used). Clearly, this
scale will vary depending on the organism size-fraction
considered, being smaller for bacteria than for urchins.
Gamma diversity is the total diversity of a region, obtained
by integrating diversity across all patch types.
Whittaker’s framework is useful for the many relevant
scales (centimeters to hundreds of kilometers) but also reflects a fundamental difference in pelagic and benthic realms.
Benthic ecologists, who tend to focus on habitat comparisons
and the associated communities, usually sample alpha diversity and sometimes extrapolate from these samples to estimate gamma diversity. The sampling units for most pelagic
studies (plankton tows) often cut across multiple patches in
the fluid and dynamic water column and thus may sample
gamma rather than alpha diversity. Indeed, pelagic biologists
are more comfortable stating numbers of species in a given
area of the ocean than are benthic ecologists, who recognize
that very few bottom areas have been sufficiently sampled
for them to be confident that rare species have not been
missed.
Structural vegetation and connections
with sedimentary biota
There are approximately 50 described mangrove species
and 45 species of seagrass, but in both of these systems, a
given area typically will contain only a few relatively common species. Kelp beds, which occasionally have associated
sedimentary habitat, are also dominated by only a few plant
species, although globally there are thousands of macroalgal species. There is evidence from research on seagrass
(Edgar 1983), mangal (Gee and Somerfield 1997), and salt
marsh ecosystems (Levin and Talley, in press) that different
fauna tend to be associated with different vegetation types
both above and below the SWI. However, the above SWI diversity of structural plants within a given location in the marine environment is relatively low, with one or only a handful
of species represented, and even within these groups there
is often zonation of species with tidal and salinity variation.
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Teasing out relationships between structural vegetation
and sedimentary fauna is therefore difficult because the
environmental conditions that regulate distribution of vegetation may be more important in regulating the associated
fauna than the vegetation itself. For example, Hutchings et
al. (1991) found greater similarity between infauna associated with different seagrass species within one patch than between those associated with the same species of seagrass in
different patches. Similarly, Collett et al. (1984) demonstrated that local environmental conditions determine the
macroinfaunal composition associated with the seagrass
Posidonia australis along the Australian coast. As a result of
overriding environmental variables, the species pool associated with a patch of a given seagrass is often much smaller
than that associated with that seagrass species over a broader
scale. Further evidence for an absence of a direct diversity linkage between above-sediment structure and below-sediment
biota was found in a Fiji lagoon where above-SWI structural
composition is a poor predictor of below-sediment diversity (Schlacher et al. 1998). In summary, there are potential
linkages between species associated with structural vegetation and the sediment beneath (Figure 1), but evidence
suggests that linkages are coincidental in that both communities are affected by similar environmental variables. One
complication in linking above- and below-SWI species
numbers and composition is seasonal and annual variability in below-SWI organisms.
Structural vegetation:
Water column-down linkages
Although specific biodiversity links are poorly documented,
there are numerous examples of above-SWI vegetation
structuring the sedimentary environment below. Sediment
trapping and water flow baffling by structural vegetation can
often alter the grain size of sediments near the vegetation.
Given that sediment grain size is a major delimiter of infaunal
distribution, there should be a clear linkage of structural vegetation to below-SWI biodiversity and composition. Productivity of vegetated habitats often exceeds that of adjacent
areas. Stimulation of microbial growth by root exudates
may enhance resources and diversity of nematodes and
other below-SWI organisms, particularly in seagrasses (Osenga and Coull 1983). A recent study found little variation
in sedimentary species colonizing litter from different mangrove species but some differences depending on which living mangrove species the litter was associated with (Gee and
Somerfield 1997). Variability in sedimentary fauna was attributed to the root structure and geochemistry of the mangrove species. Structural vegetation can also depress diversity;
large detrital production, combined with the reduced water flow often observed in mangals and salt marshes, can lead
to organic loading and reduced sediment oxygen availability (Alongi 1997) with a subsequent depression of below-SWI
species richness. Indeed, the geochemistry of structuralvegetation habitats is markedly different from that of nonvegetated areas as a result of increased productivity,
increased sedimentary nutrients, and a greater propensity for
anoxia related to the large amounts of detritus produced.
Structural vegetation influences food webs at many
levels. Many primary producers, particularly vascular plants,
produce “signature” compounds including lipids, polysaccharides, and antiherbivory chemicals that may favor specific
bacterial and fungal populations; the effects of these compounds may have ramifications up through the food chain.
The tannin-rich detritus produced in mangals, for example,
is used by a tannin-tolerant fauna with low composite
diversity (Alongi and Christoffersen 1992). But for macrofaunal species able to cope with productive environments such
as mangals, competitors are presumably few and organic
matter is abundant.
Habitat complexity generally enhances diversity in biological communities, and structural vegetation and root
structures provide critical habitat for a diversity of species
(Figure 1). An increase in above-SWI macrofaunal richness and composite diversity in seagrass sediment communities has been linked to abundance and numbers of species
of seagrass on regional and latitudinal scales (Stoner and
Lewis 1985). Species richness of infauna within vegetated areas is elevated in comparison with that of adjacent bare
sand habitat. (See Peterson 1979 for macrofauna, defined as
organisms retained on a 300- or 500-µ sieve; Boucher 1997
for meiofauna, defined as organisms retained on a 40-µ
sieve.) The explanation for this pattern is that predators
tend to depress diversity in soft-sediment systems at small
scales, and seagrasses may provide a predation refuge (Peterson 1979). The structural complexity of sediments within
salt marshes and mangals cannot be used by many species
because of the variability in salinity, temperature, exposure, and oxygenation in coastal habitats. In mangals, for example, the below-SWI community is often reduced in
diversity relative to adjacent nonvegetated subtidal sediments (Gee and Somerfield 1997). Habitat complexity may
also have negative effects on species; the roots of seagrasses
and marsh grasses likely exclude some burrowers, tube
builders, and infauna (Levin and Talley, in press).
Predators living above the SWI may, in some instances,
prey upon infauna. Caging experiments focusing on meiofauna living in mangal sediments suggest that the impact
of predation on infauna is modest, and the predator and
prey communities operate largely independently (Schrijvers
et al. 1995). Salt marsh microcosm experiments with grass
shrimp indicated that although the shrimp reduced meiofaunal densities, Shannon–Weiner diversity was largely unaffected (Bell and Coull 1978). It is possible that predation
effects in these habitats, like those described below, may
prove more important in terms of habitat modification
than for predation per se. These findings contrast with the
seagrass studies described above, suggesting no simple relationships between predators, vegetative structure, and
infaunal diversity.
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Structural vegetation:
Sediments-up linkages
The effects of below-SWI organisms on above-SWI organisms are likely to be indirect and therefore difficult to document. Microbes living within sediments are critical for
mineralization of detritus generated by vegetation; they
provide nutrients to roots and above-SWI components of
the vegetation (Alongi 1997). Burrowing by macrofauna
can improve sediment aeration with positive effects on
mangrove growth (Smith et al. 1991), likely through alteration of porewater sulfide and ammonium concentrations.
Although one might predict that burrowers would enhance
microbial biomass and diversity within sediments, few data
suggest an effect on above-sediment diversity. In coastal
ecosystems, and particularly coral reefs, organisms that
migrate out of sediments at night can be a significant component of the above-SWI fauna (Sorokin 1993), providing
a possible opportunity for interaction between above- and
below-SWI organisms. Infaunal grazers on seedlings and
root structures can also regulate mangrove distributions (see
Tomlinson 1986). These examples of bottom-up effects in
vegetative systems do not link to biodiversity per se and often involve individual species–species or trophic group interactions. Whether the lack of evidence for bottom-up
effects of biodiversity on structural vegetation reflects an absence of interaction or simply inadequate data is difficult
to say.
Linkages in coastal areas lacking
structural vegetation
Many coastal areas lack obvious physical structures, such as
those associated with structural vegetation, although reefs
created by polychaete worms and bivalves and other biogenic
structures, such as feeding pits and tubes, may fill a similar
role. Aside from these structures, potential effects of aboveSWI diversity on below-SWI diversity in most areas are
likely to be expressed through productivity, predation and
associated sediment disturbance (bioturbation), and recruitment processes. In some shallow areas, benthic diatoms and cyanobacteria may form mats on top of sediments
that can influence rates of nutrient exchange between sediments and the overlying water column (Sundbäck and
Granéli 1988). But for most marine sediments, light is attenuated or lacking at the sediment surface, and primary production occurs only in surface waters. Some of this primary
production will sink to the sea floor and fuel the sedimentary system, but the structural complexity of the habitat is
not enhanced as it is in systems with structural vegetation.
Epifaunal species, such as sponges and anemones, form
above-sediment structures, but given that epifaunal organisms do not usually occur over the large spatial scales and
high densities typical of many vegetated areas, the scale of
impact is probably reduced. Coral and coralline algal reefs
are notable exceptions, but these communities include
mostly nonsedimentary species. Nonetheless, even nonvegetated sedimentary habitat has a three-dimensional
1080 BioScience • December 2000 / Vol. 50 No. 12
spatial structure that affects benthic composition, as seen in
studies of trawling impacts (Hutchings et al. 1991).
Studies to test specifically the hypothesis that productivity, predation, and recruitment may be related to above-SWI
species richness and composite diversity are virtually nonexistent, but some qualitative comparisons can be made, and
compelling data suggest the existence of linkages. Longterm pelagic and benthic data sets from the North Sea suggest that changes in biomass and species abundance have
occurred in both habitats since the 1970s, but linkages between community structure of habitats are weak (Austen et
al. 1991).
Above-SWI productivity may impact sedimentary diversity through three potential routes. Amounts of organic
loading, timing, and biochemical composition of products
of photosynthesis all can affect sedimentary organisms and
their composition. When productivity is extremely high
(such as under organic loading), macrofaunal (Pearson and
Rosenberg 1978) and meiofaunal (Coull and Chandler
1992) richness and composite diversity are often depressed,
but these changes relate to hypoxia resulting from increased
productivity rather than to changes in pelagic diversity per
se. Increasing areas of ocean bottom are experiencing hypoxic
events that can cover thousands of km2 of sea floor and eliminate most resident fauna (Malakoff 1998). Toxic algal
blooms can have a similar impact.
The anticipated impact of variability in organic loading
on sedimentary diversity is even more tenuous. Schratzberger
and Warwick (1998) demonstrated in microcosm experiments that continuous inputs at moderate levels promote
greater nematode diversity than episodic inputs. By contrast,
temporal variability in resource supply, combined with nonlinear responses of different species to resources, is one
model to explain high species richness and composite diversity in the deep sea (Grassle and Sanders 1973). Comparison of microbial diversity in shallow and deep tropical
and temperate systems with that in deep pelagic systems
could provide further insight into the role of variability in
resource supply by testing whether microbial diversity is affected by differences in seasonality and the pulsed or episodic
nature of organic inputs.
Biochemical diversity of organic inputs from above the
SWI could affect diversity of microbial and potentially
meiofaunal and macrofaunal taxa (Dauwe et al. 1998). Major groups of primary producers, including various groups
of phytoplankton, macroalgae, and vascular plants in shallow systems, produce specific polysaccharides or lipids that
can favor specific species of hydrolytic bacteria (Percival
and McDowell 1967). For example, the capacity for hydrolysis of agaropectin and carrageenans, compounds produced by red algae, is limited to relatively few bacterial taxa.
Thus, inputs of these polymers may affect both the diversity
and biogeography of below-SWI bacteria. The nature of
polysaccharide inputs, including contributions from terrestrial systems, might also play a role in the diversity and
relative importance of fungi, some of which possess unique
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hydrolytic capabilities. Because proteins, nucleic acids, and
lipids are ubiquitous, they are probably less important than
polysaccharides in determining benthic microbial diversity. Distinctive groups of bacteria from species to phylum
levels of organization also exhibit substrate preferences for
proteins, sugars, lipids, etc., and the relative abundance of
polymer classes may therefore affect microbial functional diversity. Abundance of polymer classes varies with planktonic
species composition, terrestrial organic loading, and water
column depth. Thus, there is good reason to believe that
above-SWI diversity will affect below-SWI bacteria and
perhaps fungi, but whether this linkage extends to below-SWI
meiofauna and macrofauna remains untested. One might
predict that higher diversity low in the food chain (i.e., bacteria) could enhance diversity in larger organisms if food diversity enhances feeder diversity. Given the limited data
available on diversity of microbial groups, however, we acknowledge the highly speculative nature of these hypotheses and offer them as ideas to motivate research directions.
Evidence suggests that predation and disturbance by
above-SWI epifaunal predators (e.g., crabs, shore birds,
flatfish) can affect diversity by removing individuals but
also through habitat modification. Caging studies suggest
that predators reduce macroinfaunal diversity (Peterson
1979), presumably because they often selectively remove
slow-growing and vulnerable species. Because these conclusions are drawn from caging studies rather than direct
comparisons of above- and below-SWI diversity, they tell us
little about changes at scales larger than the cages, but they
do suggest that above-SWI diversity can have a direct impact
on below-SWI diversity at small scales.
It is likely that the greatest effect of predation on species
diversity is through habitat modification; the habitat heterogeneity that predators may introduce can result in enhanced diversity at larger scales. Large and mobile above-SWI
bottom feeders, such as rays, tend to cause an initial depression of local diversity as they remove prey and physically
disturb the sediment, sometimes followed by transient increases in species richness or evenness, enhancing diversity
(VanBlaricom 1982). This sort of biological disturbance
opens up habitat and eliminates most species, resulting in
a succession through an initial low-diversity stage dominated
by a few opportunistic or “weedy” species, an intermediate
stage characterized by high diversity because opportunists
and background species co-occur, and finally a moderatediversity, late stage in which opportunists have declined
and background species again dominate. A similar sequence
occurs when pelagic carcasses fall to the bottom, providing
food and a localized disturbance benefiting species that are
not abundant otherwise (Smith et al. 1998). Thus, although
diversity at the local (sample) scale may often be reduced,
species numbers at the landscape scale may be enhanced. Interestingly, most of what we know about predation is from studies of above-sediment species, rather than interactions
among infaunal species. This raises the intriguing question of whether there are fundamental differences in the
effects of above-SWI versus infaunal predators on sedimentary biodiversity.
Large sediment diggers above the SWI, such as rays (VanBlaricom 1982), crabs, and shrimp, may also affect sedimentary community diversity through geochemical
mechanisms. For example, sediment disturbance, such as
from burrowing polychaetes (e.g., Kristensen et al. 1985), can
introduce oxygen into anaerobic sediments (Aller 1982), and
above-sediment diggers will have a similar effect. Burrows
may also help concentrate organic matter through deposition or active sequestration by organisms that live within the
burrows. Alternatively, burial of organic detritus can result
in increased sediment oxygen demand and production of
compounds rich in organic material. Clearly, these activities
will influence microbial, meiofaunal, and, most likely, macrofaunal diversity, but studies explicitly addressing geochemical effects on diversity are lacking (although see Soetaert and
Heip 1995). As an analog to predator disturbance, animal
burrows produce biogeochemically distinct conditions
that may be used by specific microbial and meiofaunal
populations (Dobbs and Guckert 1988). For example, dehalogenating populations may be enriched in burrows of
haloorganic-producing enteropneusts (King 1988). Although it is clear that animal–microbe interactions may be
responsible for unique microbial associations with burrows, planktonic diversity could provide an indirect control
on microbial diversity in sediments because benthic biogeography is likely related to composition and processes
within the plankton.
The co-occurrence of the pelagic stage of some benthic
species with holoplanktonic species provides ample opportunity for interaction in the water column. Many benthic species produce planktonic larval stages that may spend
anywhere from minutes to months in the water column, potentially interacting with a broad suite of holoplanktonic
species through predation or competition for food. The
dispersal stages of benthic species usually experience very
high levels of mortality, but whether diversity of the plankton plays a role in rates of mortality is untested. For example, greater diversity of predators could increase the
likelihood that meroplankton will suffer from predation.
Mesocosm experiments offer one approach to test these
hypotheses.
Coastal habitats lacking structural
vegetation: Sediments-up linkages
Functional groups within sediments can affect abovesediment diversity via selective transfer of matter through
the SWI, particle exchange through biological mechanisms
(feeding of pelagic species on the benthos and vice versa, migrations from benthic species into the water column including reproductive propagules), and release of dissolved
substances after mineralization of organic matter or transformation of pollutants in sediments (Henriksen et al.
1983).
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Nutrient regeneration is critical in fueling coastal productivity above the SWI interface, and sedimentary microbes play a key role in the regeneration process (see
Snelgrove et al. 1997). In tropical areas, this seasonal effect
is less pronounced, and benthic algae may capture most
nutrients as they diffuse out of sediments (Alongi 1997). The
feeding, movements, and respiration of macrofaunal taxa affect the porewater concentrations and availability of oxygen,
nitrate, sulfate, and other electron acceptors in marine sediments, which in turn affects carbon and nitrogen remineralization rates by microbes (Rhoads et al. 1978). The
influences of regeneration rates on diversity are undoubtedly complex, but high regeneration can result in blooms of
a few dominant phytoplankton species. Rates of regeneration and their temporal variation can affect phytoplankton
composition and diversity. Pulsed areas often have a few
dominant phytoplankton species at any one time, but less
temporally variable areas may be more species rich unless
nutrient levels are highly elevated.
Pollutants, much like regenerated nutrients, are affected
by microbial diversity and macrofaunal activity that influence the magnitude and timing of release of modified and
untransformed pollutants from sediments into the water column. Impacts may be direct, such as when pollutants bound
to sediment particles are moved by macrofauna so that they
become deeper or shallower in the sediment horizon, or linkages may be less direct. For example, when macrofauna colonize polluted sediments, their reworking typically changes
redox conditions and enhances porewater efflux from sediments, triggering release of heavy metals. Degradation of
organic pollutants may also depend on the presence of
specific microorganisms (e.g., Geiselbrecht et al. 1996),
which may in turn depend on macrofaunal activities. Linkages between the nature and magnitude of pollutant release
from sediments and pelagic biodiversity are undoubtedly
complex, and a descriptive framework does not exist, but
species-specific transfers and pollutant effects are known.
Demersal fish that feed on the benthic organisms such as
shrimp and polychaetes, provide an obvious conduit for sediment contaminants (e.g., heavy metals, PCBs) to the aboveSWI domain.
Active vertical migration at night for feeding and reproduction characterizes some adult meiobenthic (Armonies
1988) and macrobenthic species that migrate from below the
SWI interface up into the water column (Sorokin 1993).
Adults of benthic species will leave sediments at night and
make excursions into the water column, but interactions with
the above-SWI fauna have not been well studied (Mees and
Jones 1997). Often, they are eroded from the sediment by
strong bottom currents generated by wind or tides, but
mollusks and polychaetes are also known to move after
metamorphosis, perhaps in search of better food (Olivier et
al. 1996). The effects of these excursions and interactions with
the above-SWI fauna have not been quantified, but these
benthic migrants lengthen the list of taxa found in the water column.
1082 BioScience • December 2000 / Vol. 50 No. 12
Meroplankton, the pelagic larvae that are produced by
many macrobenthic species in coastal areas, remain in the
plankton for hours, weeks, or even months, depending on
the taxon. The meroplankton on continental shelves often
dominate the holoplankton (wholly planktonic organisms)
during a large part of the year, and different species tend to
peak at different times of year, particularly in the spring and
autumn, when phytoplankton blooms occur. The effects of
meroplankton grazing on phytoplankton are expected to be
considerable. Meroplankton can also be an important food
source for water column species, and meroplankton diversity could impact holoplankton diversity and pattern. An intriguing example is seen in the North Sea, where long-term
plankton data indicate that meroplankton have become the
dominant taxon in shelf waters in recent years, with corresponding decreases in the formerly abundant copepods
(Lindley et al. 1995). This change has been linked to increases
in biomass of benthic echinoderms, which in turn may be
related to eutrophication or fishing disturbance (Duineveld
et al. 1987). Whether increases in meroplankton are responsible for the decline in holoplankton is impossible to determine without experimental data, but the pattern raises
interesting questions on above- and below-SWI linkages.
How changes in species composition affect the ecosystem will
be difficult to determine, given the confounding impacts of
fishing disturbance, pollution, and climatic factors that influence the North Sea ecosystem. Fishing impacts on sedimentary fauna remain a difficult question to address in any
ecosystem, given that virtually any area that can be fished has
been fished, and unimpacted “control” areas either are entirely lacking from a region or represent fundamentally different habitats that also happen to be untrawlable. Smith et
al. (2000) discuss fishing impacts in greater detail.
Suspension feeding activity by benthic organisms provides
a mechanism of interaction between pelagic and benthic systems (Officer et al. 1982). Suspension feeders often transfer
much larger quantities of material to sediments than would
be possible by sedimentation alone, and they may deplete the
lower water layers of particles and increase transparency
(Butman et al. 1994). The intriguing example of the Asian
clam, Potamocorbula amurensis, and the effects of its introduction into San Francisco Bay, are discussed by Smith et al.
(2000). Elmgren and Hill (1997) point out that despite
much lower diversity in the Baltic Sea, ecosystem processes
such as carbon cycling and trophic transfer occur as they do
in the North Sea (Steele 1974), suggesting that total diversity may not be important to these processes. But in one area
of the Baltic where suspension feeders are absent, energy flow
is markedly different, with reduced phytoplankton flux to the
benthos and reduced importance of macrofauna relative
to meiofauna. How the absence of suspension feeders affects
pelagic processes remains unclear, but primary productivity and fisheries yields are both considerably reduced in
this area.
Resting stages in the form of eggs and cysts are produced
by a number of pelagic phytoplankton and zooplankton
Articles
species, and these stages can be abundant in coastal sediments
(Marcus 1996). Among the best known of these are dinoflagellate cysts, which serve as a hardy resting stage and
can seed toxic blooms, leading to paralytic shellfish poisoning
through ingestion of toxic dinoflagellates by suspension-feeding bivalves. During unfavorable conditions, the sediments
provide a refuge for resting stages of various taxa, which may
become active when conditions become more favorable or
storm events resuspend them (e.g., Marcus and Boero 1998).
Emergence from sediments may be suppressed by anoxia,
darkness, or physical contact with the sediment and may
therefore be affected by the bioturbation activities of belowSWI organisms. Copepod eggs, for example, are extremely
hardy and can pass through digestive tracts of macrofauna
unharmed, although predation by meiofauna may occur.
Resting stages may be relocated by dredging activities or in
guts of organisms that are transplanted for aquaculture.
Sediments may also provide refugia for other pelagic organisms such as fungi, viruses, and parasites. (See discussion
of the predatory dinoflagellate Pfiesteria piscicida in Smith
et al. 2000). The linkage to above-SWI diversity is very tentative, but removal of key fish predators is likely to affect
pelagic food chains.
The benthos can be an important food resource for aboveSWI organisms. Changes in size and species composition of
infauna, such as after chronic bottom trawling or shortterm anoxia events resulting from eutrophication, influence above-SWI species feeding at the sediment-water
interface. Bottom-feeding fishes that depend on infauna
may then switch to other prey or migrate elsewhere (Feder
and Pearson 1988). As described above, a variety of aboveSWI species feed on below-SWI organisms, including many
that contribute to important commercial fisheries.
Linkages in the open ocean
Within the open ocean, a significant portion of the water column is spatially decoupled from the sediment-water interface, and most organisms living near the ocean’s surface
have no direct contact with the sediment. Unlike the
nearshore environment described above, there is no primary
production near the bottom, and the exchange of dissolved
materials, including nutrients and dissolved gases, is extremely slow relative to biotic lifetimes. The water column
depths involved may be several kilometers, and vertically migrating predators span the full water column only in shallower areas. Thus, linkages between diversity in the aboveand below-SWI fauna are likely to be even less direct than
in other marine systems, although the potential mechanisms have some similarities. This decoupling presents
problems in defining biogeographical provinces (e.g., Angel 1997), which, though well defined in shallow water and
open-ocean surface waters, are probably blurred in deeper
water, where temperature and light are less variable.
A number of studies have suggested that latitudinal diversity patterns exist in above- and below-SWI communities. Although ocean currents and wind patterns greatly
complicate simple generalizations, it has been suggested
that phytoplankton diversity decreases toward higherproductivity areas as a few dominant species take over. Data
from McGowan and Walker (1985) suggest a general decrease
in pelagic copepod diversity with latitude within the North
Pacific, although regional oceanography blurs any simple
trend. Angel (1997) suggests a decline in diversity with increasing latitude in the North Atlantic for several pelagic animals, a pattern seen to at least 2000 m depth. In general, this
pattern is consistent with macrofaunal shallow-water and
deep-sea data, but it contradicts patterns in nematodes
(Figure 2a). Although it is tempting to suggest that the diversity of pelagic organisms that provide food for the benthos may be linked to the diversity of below-SWI organisms,
the patterns represent a weak correlation.
Another pattern that can be compared between above- and
below-SWI communities is the relationship with depth.
Rex et al. (1997) reviewed depth-related patterns in the below-SWI fauna and observed highest diversity at intermediate depths of approximately 2000 m. Other studies have
also observed peaks at intermediate depths, although peaks
are not necessarily at the same depths. Local diversity of phytoplankton tends to increase with depth until light becomes
limiting. Zooplankton diversity may also reach a peak at intermediate depths in the North Atlantic (Angel 1997;
Figure 2b). Water column diversity has also been compared
along a transect running perpendicular to shore (Angel
1997) and suggests a pattern of low diversity across shelf
depths, a peak at the shelf break, and a decline over the
continental slope (Angel 1997); the sampling transect did not
extend to mid-continental slope depths where Rex et al.
(1997) observed a diversity peak. There are also intriguing
examples of high-diversity shelf habitats (Gray et al. 1997),
illustrating the need for better sampling coverage to achieve
generalizations.
Although there are some similarities in patterns of aboveand below-SWI communities over broad spatial scales
(Boucher and Lambshead 1995, Angel 1997), there is little
evidence for cause and effect. It is equally plausible that
similar processes (e.g., productivity, energy) affect above- and
below-SWI biota similarly and that diversity patterns are unrelated. Geological history (e.g., Jablonski 1993), which may
have similar consequences for above- and below-SWI organisms, adds further complication.
The open ocean:
Water column-down linkages
Productivity is the most likely mechanism by which aboveSWI organisms affect the sedimentary infauna living in the
highly food-limited deep sea. Materials sinking from surface
waters fuel the benthos far below, and it is possible that
patterns in the deep-sea benthos may be linked to diversity
and temporal variability in food resources. There is ample
evidence that food pulses support a somewhat-specialized
subset of species in this environment, and there is some evidence that different food resources may support different
December 2000 / Vol. 50 No. 12 • BioScience 1083
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Figure 2a. Patterns of diversity with
latitude for a variety of pelagic and
benthic taxa. Sources of data are Roy
et al. (1998) for shallow gastropods,
Angel (1997) for ostracods, Rex et al.
(1993) for deep-sea gastropods and
isopods, Lambshead et al. (2000) for
nematodes, and Pierrot–Bults (1997)
for euphausiids. Different sampling
intensities and measures were used in
different studies so that comparison
should be only between patterns in
different groups rather than between
samples.
(°)
Figure 2b. Changes in diversity with
depth for benthic and pelagic taxa.
Ostracod data are from Angel (1997),
and gastropod data are from Rex et al.
(1997). Again, different sampling
intensities and measures were used in
different studies so that comparison
should be only between patterns in
different groups rather than between
samples.
faunas (Snelgrove et al. 1992). Benthic infaunal species also
aggregate, possibly because detritus distribution is not uniform or because different types of detritus might attract different types of species. One current theory is that small-scale
patchiness in food supply is critical in promoting deep-sea
diversity (Grassle and Sanders 1973). But again, it is unclear
whether diversity of food resources (and thus pelagic diversity) makes any real difference. There is some congruence
in global-scale patterns of surface productivity and deep-sea
biodiversity patterns that suggests ecological coupling
through the water column (Rex et al. 1993). The bathymetric diversity pattern has been related to a gradient in productivity that decreases from the coast to the deep ocean.
There is sufficient benthic and pelagic biodiversity data to
begin testing this idea more thoroughly.
1084 BioScience • December 2000 / Vol. 50 No. 12
Correlative linkage between broad-scale surface productivity and benthic diversity can be tested with existing data
on global export production (Falkowski et al. 1998) and regional studies of infauna. Plotting species counts for different taxa on Falkowski et al.’s estimates for carbon export
suggests that there may indeed be a relationship between
productivity and diversity for some taxa, with a decline in
diversity as productivity increases. (Figure 3; Table 1. See also
Watts et al. 1992 for a more detailed analytical approach.)
Whether this pattern relates to amounts, or to variability, of
carbon export is difficult to judge since sample sizes are
small and many highly productive areas are also quite seasonal. Unfortunately, the spatial coverage that has been
achieved in the sampling of benthic organisms in the oceans
is insufficient to be certain that such relationships exist.
Articles
Figure 3. Estimates of deep-sea diversity for various taxa superimposed on an image of global carbon export pattern as
estimated by Falkowski et al. (1998). Carbon export image reproduced from Falkowski et al. (1998). Numbers in red are
nematode species counts from Lambshead et al. (2000), numbers in white are shallow mollusk species counts from Roy et al.
(1998), and numbers in black are expected species in sampling 50 individuals from Rex et al. (1993). Because of different
sampling intensities and measures used, comparison should be only between patterns in different groups rather than
between samples.
Again, the importance of above-sediment diversity, as opposed to productivity, is unclear.
Predation effects in the deep sea, and particularly effects
on diversity, are not well understood. Predation by aboveSWI organisms was one of the first processes suggested to
be important in structuring deep-sea biodiversity (Dayton
and Hessler 1972), although shallow-water data suggest
that predators depress diversity at small scales. The role of
predators in creating disequilibria that were described for
shallow water has a similar potential application here. There
is little evidence that pelagic predators feeding on infauna
are particularly selective with respect to species composition,
but successional mosaics may be created by patchy predation. Recent caging experiments in the San Diego Trough
(Eckman et al. 1999) tested the role of predation in maintaining deep-sea diversity. No studies have been designed to
test whether the diversity of these predators is significant for
infaunal communities. Another possible effect of predation occurs during the reproductive phase, when some deepsea species release reproductive propagules into surface
waters, where they may be subject to predation or competition with pelagic species. The magnitude of this impact is
difficult to evaluate, but given the lesser importance of
planktotrophic larvae in the deep ocean than in shallow
water and the large spatial decoupling involved, a diversity
linkage seems unlikely. One final point regarding deep-sea
predators is that many are essentially decoupled from surface waters, where production takes place. Although some
species make extensive diel migrations, many deep-sea
predators are more tightly coupled to the benthos than they
might be in shallow water.
Habitat complexity in the deep sea is considerably less than
in shallow water, with bioturbation, predation, and food
flux contributing to benthic diversity through creation of
December 2000 / Vol. 50 No. 12 • BioScience 1085
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Table 1. Correlational relationships among latitude, productivity export,
and diversity.a
How can above–below SWI
linkages be more effectively
tested?
Given the potential relationships outlined above
and the current interest in biodiversity, it is
critical that we strive for a better understanding
Deep-sea gastropods
Latitude
–
0.612
–0.591
of how above- and below-SWI diversity are
Productivity
0.180
–
–0.888
linked in the oceans before too many of these
habitats and their linkages are unwittingly alDiversity
0.216
0.002
–
tered by human disturbance. Determining inShallow-water mollusks
Latitude
–
0.631
–0.798
teraction of above- and below-SWI diversity is
a great challenge. Analysis of natural patterns
Productivity
0.280
–
–0.840
with more complete spatial coverage globally, inDiversity
0.053
0.027
–
cluding areas with unusual characteristics, will
clarify whether latitude, productivity, and depth
Deep-sea nematodes
Latitude
–
0.534
0.225
influence diversity within the pelagic and benProductivity
0.824
–
0.561
thic domains. Experimental studies will be necessary to determine causality within domains
Diversity
1.00
0.741
and will be critical for linking above- and belowSWI diversity. An obvious means of testing the
importance of diversity in one domain relative
to the other is to manipulate diversity in one and
a
These analyses are based on different types of diversity estimates as described and
monitor response in the other. Unfortunately,
from the same sources as in Figure 3, and approximate measures of productivity
manipulation of sedimentary habitats is extraexport as extracted from the color image in Falkowski et al. (1998). As such, this
ordinarily difficult because removal of specific
should be treated as an exploratory analysis designed to stimulate more rigorous comgroups of organisms usually disturbs the sediparisons. Values above dashes are Pearson correlation coefficients, and those below
ments and alters basic geochemistry. Baited
dashes are Bonferroni-adjusted probability values with significant values shown in
bold. It should be noted that more detailed analysis by Lambshead et al. (2000) has
traps and selective poisoning offer one approach
indicated a significant positive relationship between productivity and deep-sea nemato “removing” certain groups. It is also feasible
tode species richness.
to build on caging experiments by excluding
pelagic species either completely or selectively,
allowing effective in situ tests of impacts. The
importance of organic-matter diversity could
microhabitat. As mentioned earlier, it is thought that
also be tested by manipulating the types of food resources
micropatches create habitat heterogeneity that is critical in
supplied to sediments and below-SWI organisms.
promoting deep-sea diversity; thus, a greater diversity of
Mesocosms, where species composition can be carefully
predators, bioturbators, and food types should create a
regulated in the above- and below-SWI communities, offer
greater diversity of patch types and therefore a greater diversity
another effective means of studying above–below processes
of benthos (e.g., Snelgrove et al. 1992). Sediment diversity has
(e.g., Widdicombe and Austen 1998). The trick is to strike
been shown to be a significant predictor of biological divera balance between ease of control and maintaining a
sity in the deep sea (Etter and Grassle 1992), suggesting that
“natural” ecosystem. In short, the linkages between abovehabitat is indeed important to deep-sea organisms on many
and below-SWI diversity have received little attention, and
scales. However, linkages of diversity and habitat patchiness
are an area where many research opportunities exist and
have not been broadly established.
many questions remain to be answered.
Latitude
Productivity
The open ocean: Sediments-up linkages
As indicated earlier, there are likely very few bottom-up effects of open-ocean infauna, although their role in global carbon (benthic mineralization) and nitrogen (denitrification)
cycles may be underestimated (Heip et al., in press). The huge
scales involved suggest that biodiversity likely plays a minor
role, except perhaps in terms of functional groups. As in shallow systems, some benthic species produce pelagic larvae. But
low faunal densities in the deep sea suggest that reproductive propagules will be few and their impact on aboveSWI organisms minimal.
1086 BioScience • December 2000 / Vol. 50 No. 12
Diversity
Acknowledgments
We wish to thank to Diana Wall for her leadership in tackling soil and sediment biodiversity. We also thank the SCOPE
Committee on Soil and Sediment Biodiversity and Ecosystem Functioning; an anonymous US foundation; and the
Ministries of Agriculture and the Environment, The Netherlands, for providing funds to host the workshop “The
Relationship between Above- and Belowsurface Biodiversity
and Its Implications for Ecosystem Stability and Global
Change” in Lunteren, The Netherlands. The efforts of Gina
Adams in orchestrating the workshop that led to this
Articles
synthesis are also greatly appreciated. Thoughtful reviews by
Rebecca Chasan, Paul Dayton, Diana Wall, and three anonymous reviewers improved this manuscript and are much
appreciated.
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